Antibody-dependent enhancement of severe dengue disease in humans

For dengue viruses 1 to 4 (DENV1-4), a specific range of antibody titer has been shown to enhance viral replication in vitro and severe disease in animal models. Although suspected, such antibody-dependent enhancement of severe disease has not been shown to occur in humans. Using multiple statistica...

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Published in	Science (American Association for the Advancement of Science) Vol. 358; no. 6365; pp. 929 - 932
Main Authors	Katzelnick, Leah C., Gresh, Lionel, Halloran, M. Elizabeth, Mercado, Juan Carlos, Kuan, Guillermina, Gordon, Aubree, Balmaseda, Angel, Harris, Eva
Format	Journal Article
Language	English
Published	United States American Association for the Advancement of Science 17.11.2017 The American Association for the Advancement of Science
Subjects	Adolescent Animal diseases Animal models Antibodies, Viral - blood Antibodies, Viral - immunology Antibody-Dependent Enhancement Aquatic insects Child Child, Preschool Children Cohort Studies Complications Dengue - blood Dengue - immunology Dengue - virology Dengue fever Dengue hemorrhagic fever Dengue Vaccines - immunology Disease Disease transmission Female Fever Humans Immune response Male Pathogenesis Vaccine development Vaccines Vector-borne diseases Viral diseases Virology Viruses
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Abstract	For dengue viruses 1 to 4 (DENV1-4), a specific range of antibody titer has been shown to enhance viral replication in vitro and severe disease in animal models. Although suspected, such antibody-dependent enhancement of severe disease has not been shown to occur in humans. Using multiple statistical approaches to study a long-term pediatric cohort in Nicaragua, we show that risk of severe dengue disease is highest within a narrow range of preexisting anti-DENV antibody titers. By contrast, we observe protection from all symptomatic dengue disease at high antibody titers. Thus, immune correlates of severe dengue must be evaluated separately from correlates of protection against symptomatic disease. These results have implications for studies of dengue pathogenesis and for vaccine development, because enhancement, not just lack of protection, is of concern.
AbstractList	For dengue viruses 1 to 4 (DENV1-4), a specific range of antibody titer has been shown to enhance viral replication in vitro and severe disease in animal models. Although suspected, such antibody-dependent enhancement of severe disease has not been shown to occur in humans. Using multiple statistical approaches to study a long-term pediatric cohort in Nicaragua, we show that risk of severe dengue disease is highest within a narrow range of preexisting anti-DENV antibody titers. By contrast, we observe protection from all symptomatic dengue disease at high antibody titers. Thus, immune correlates of severe dengue must be evaluated separately from correlates of protection against symptomatic disease. These results have implications for studies of dengue pathogenesis and for vaccine development, because enhancement, not just lack of protection, is of concern. Dengue fever is caused by a mosquito-transmitted flavivirus resembling Zika virus. Both viruses can cause severe diseases in humans with catastrophic sequelae. It has been suspected in humans, and shown in animal models, that the host's immune responses can make disease worse. Katzelnick et al. examined data from a long-term study of Nicaraguan children exposed to dengue virus (see the Perspective by Feinberg and Ahmed). They confirmed that antibody-dependent enhancement of disease occurs at a specific range of antibody concentrations. Low levels of antibody did not enhance disease, intermediate levels exacerbated disease, and high antibody titers protected against severe disease. These findings have major implications for vaccines against flaviviruses. Indeed, recent vaccine trials have shown evidence of severe disease in some recipients who were previously exposed to virus.Science, this issue p. 929; see also p. 865 For dengue viruses 1 to 4 (DENV1-4), a specific range of antibody titer has been shown to enhance viral replication in vitro and severe disease in animal models. Although suspected, such antibody-dependent enhancement of severe disease has not been shown to occur in humans. Using multiple statistical approaches to study a long-term pediatric cohort in Nicaragua, we show that risk of severe dengue disease is highest within a narrow range of preexisting anti-DENV antibody titers. By contrast, we observe protection from all symptomatic dengue disease at high antibody titers. Thus, immune correlates of severe dengue must be evaluated separately from correlates of protection against symptomatic disease. These results have implications for studies of dengue pathogenesis and for vaccine development, because enhancement, not just lack of protection, is of concern. For dengue viruses 1 to 4 (DENV1-4), a specific range of antibody titer has been shown to enhance viral replication in vitro and severe disease in animal models. Although suspected, such antibody-dependent enhancement of severe disease has not been shown to occur in humans. Using multiple statistical approaches to study a long-term pediatric cohort in Nicaragua, we show that risk of severe dengue disease is highest within a narrow range of preexisting anti-DENV antibody titers. By contrast, we observe protection from all symptomatic dengue disease at high antibody titers. Thus, immune correlates of severe dengue must be evaluated separately from correlates of protection against symptomatic disease. These results have implications for studies of dengue pathogenesis and for vaccine development, because enhancement, not just lack of protection, is of concern.For dengue viruses 1 to 4 (DENV1-4), a specific range of antibody titer has been shown to enhance viral replication in vitro and severe disease in animal models. Although suspected, such antibody-dependent enhancement of severe disease has not been shown to occur in humans. Using multiple statistical approaches to study a long-term pediatric cohort in Nicaragua, we show that risk of severe dengue disease is highest within a narrow range of preexisting anti-DENV antibody titers. By contrast, we observe protection from all symptomatic dengue disease at high antibody titers. Thus, immune correlates of severe dengue must be evaluated separately from correlates of protection against symptomatic disease. These results have implications for studies of dengue pathogenesis and for vaccine development, because enhancement, not just lack of protection, is of concern. Dengue fever is caused by a mosquito-transmitted flavivirus resembling Zika virus. Both viruses can cause severe diseases in humans with catastrophic sequelae. It has been suspected in humans, and shown in animal models, that the host's immune responses can make disease worse. Katzelnick et al. examined data from a long-term study of Nicaraguan children exposed to dengue virus (see the Perspective by Feinberg and Ahmed). They confirmed that antibody-dependent enhancement of disease occurs at a specific range of antibody concentrations. Low levels of antibody did not enhance disease, intermediate levels exacerbated disease, and high antibody titers protected against severe disease. These findings have major implications for vaccines against flaviviruses. Indeed, recent vaccine trials have shown evidence of severe disease in some recipients who were previously exposed to virus. Science , this issue p. 929 ; see also p. 865 A long-term Nicaraguan pediatric cohort reveals that a narrow range of preexisting antibody titers increases the risk of severe dengue disease. For dengue viruses 1 to 4 (DENV1-4), a specific range of antibody titer has been shown to enhance viral replication in vitro and severe disease in animal models. Although suspected, such antibody-dependent enhancement of severe disease has not been shown to occur in humans. Using multiple statistical approaches to study a long-term pediatric cohort in Nicaragua, we show that risk of severe dengue disease is highest within a narrow range of preexisting anti-DENV antibody titers. By contrast, we observe protection from all symptomatic dengue disease at high antibody titers. Thus, immune correlates of severe dengue must be evaluated separately from correlates of protection against symptomatic disease. These results have implications for studies of dengue pathogenesis and for vaccine development, because enhancement, not just lack of protection, is of concern.
Author	Harris, Eva Kuan, Guillermina Gordon, Aubree Gresh, Lionel Balmaseda, Angel Halloran, M. Elizabeth Mercado, Juan Carlos Katzelnick, Leah C.
Author_xml	– sequence: 1 givenname: Leah C. surname: Katzelnick fullname: Katzelnick, Leah C. – sequence: 2 givenname: Lionel surname: Gresh fullname: Gresh, Lionel – sequence: 3 givenname: M. Elizabeth surname: Halloran fullname: Halloran, M. Elizabeth – sequence: 4 givenname: Juan Carlos surname: Mercado fullname: Mercado, Juan Carlos – sequence: 5 givenname: Guillermina surname: Kuan fullname: Kuan, Guillermina – sequence: 6 givenname: Aubree surname: Gordon fullname: Gordon, Aubree – sequence: 7 givenname: Angel surname: Balmaseda fullname: Balmaseda, Angel – sequence: 8 givenname: Eva surname: Harris fullname: Harris, Eva
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/29097492$$D View this record in MEDLINE/PubMed
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Snippet	For dengue viruses 1 to 4 (DENV1-4), a specific range of antibody titer has been shown to enhance viral replication in vitro and severe disease in animal... Dengue fever is caused by a mosquito-transmitted flavivirus resembling Zika virus. Both viruses can cause severe diseases in humans with catastrophic sequelae....
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SubjectTerms	Adolescent Animal diseases Animal models Antibodies, Viral - blood Antibodies, Viral - immunology Antibody-Dependent Enhancement Aquatic insects Child Child, Preschool Children Cohort Studies Complications Dengue - blood Dengue - immunology Dengue - virology Dengue fever Dengue hemorrhagic fever Dengue Vaccines - immunology Disease Disease transmission Female Fever Humans Immune response Male Pathogenesis Vaccine development Vaccines Vector-borne diseases Viral diseases Virology Viruses
Title	Antibody-dependent enhancement of severe dengue disease in humans
URI	https://www.jstor.org/stable/26400863 https://www.ncbi.nlm.nih.gov/pubmed/29097492 https://www.proquest.com/docview/1975060861 https://www.proquest.com/docview/1966246742 https://pubmed.ncbi.nlm.nih.gov/PMC5858873
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